Socialite in the Dark: Do Eyes Really Matter When It Comes To Schooling?

It has been a while since I've visited the topic of blind fish. I know, I know! What took me so long, right? Well, I was browsing for fish papers, ‘cause I take care of lab fish now (I’m working my way up to Fish Whisperer status), and I came across a paper in Current Biology about the schooling behavior of cavefish, specifically the effects of eyesight loss on this behavior.

There are two main types of social “collective behavior” in fish: shoaling and schooling. Shoals are defined exclusively by social attraction, simply being near each other in a group. To form a school, individuals must also maintain coordinated body position with their schoolmates, showing polarized orientation and synchronized movement.

In a 2011 post, The Sleep of the Blind Fish, I introduced you to Astyanax mexicanus, commonly known as the Mexican cavefish or Mexican tetra. I’ll let you visit that post for more details on this species, but for today know that it has two, interfertile forms: the normal or surface form is pigmented, sighted, and has a natural photoperiod, and the blind form is albino, has no eyes, and lives in dark caves. The normal form actively groups into schools and shoals while the cave form has reduced this behavior. A study by Johanna Kowalko et al. looked to quantify this schooling behavior. To do this they made a sort of fish mobile attached to a motor. As the grouped plastic model fish on the mobile moved, the live fish had the option to join, orient with, and follow the group or not. Images and videos allowed the researchers to measure the position of the fish, average and proportion of time each fish spent with the school, and nearest neighbor distances. They found that surface fish followed the model school while cavefish did not. The surface fish swam significantly closer together than did the cavefish. Also, the cavefish showed a loss of the tendency to swim oriented to one another, or school, as well as a decreased tendency to shoal.

Greenwood et al. (2013) Fig. 1

Okay, so why is this? What do you need to do (or have) to form a group? Some type of sense, right? I mean, you need to find others of your species, be able to sense your place in the group, and be able to respond to others in your group. As we know, the cavefish have adapted to a dark environment and so have no eyes. However, they do have a increased number and distribution of taste buds and cranial superficial neuromasts (mechanoreceptors that detect movements and pressure changes in surrounding water, think lateral line or “touch”). Kowalko’s group found that surface fish have significantly fewer and smaller cranial neuromasts than do cavefish, likely an adaptation to cave life. However, they did not find this adaptation to have a large effect on the evolutionary loss of schooling. I’ll bet that your brain is jumping to the next logical conclusion: vision is important. And you would be correct. The researchers did a series of tests where they tested both types of fish in various light conditions. The surface fish actually preferred the dark, but when they were in the dark they swam farther apart and lost schooling behavior while the cavefish were unaffected by the lighting conditions.

Let’s take the next step: Is this a learned behavior or is it dependent on having eyes? It is known that cavefish develop eyes, which undergo apoptosis and degenerate. So if a surface fish were to lose its vision early in development, would it then behave like a cavefish? To test this, the researchers removed one, two, or no lenses/eyes in surface fish larvae (with some awesome microdissection skills I’m sure!), allowed them to grow up, and then tested their schooling behavior. They found that the removal of both lenses caused the fish to swim farther apart than partially-sighted (one lens) or control fish. The partially-sighted fish could follow the model school but still shoaled farther apart than did full-sighted controls.

Next, Kowalko's group wanted to see what was going on in the brain. Recent research has shown that surface and cavefish have different levels of monoamine neurotransmitters (signaling chemicals in the nervous system).  They used inhibitors to alter serotonin and monoamines. Then they ran their schooling tests. They found that serotonin levels make no difference, but preventing the breakdown of monoamines decreases schooling behavior and results in significantly greater distances between fish in the shoaling tests. These results are consistent with other evidence that a molecule involved in the synthesis of dopamine (a monoamine) affects schooling behavior in cavefish.

Finally (whew!), they performed quantitative trait locus (QTL) analysis. Basically, this is a statistical method that links the phenotype (trait) measurements and the genotype (molecular markers) to explain a genetic basis for a complex trait. They found homozygous cave alleles at a marker underlying linkage group 27 that results in a decrease in schooling behavior and a dark preference. They also found schooling QTL that does not fall in the same place as the QTL for dark preference, eye size, pupil size, or neuromast number. This means that there is are both vision-dependent and vision-independent genetic contributions to the evolution of schooling behavior. Interesting.

Is there a story here? Well, sure. Perhaps when the sighted, cavefish ancestors arrived in their new, dark homes they couldn't school because of the lack of light. Their new cave environment also had a different ecology than their surface habitat. For one, it had a lack of big predators. Schooling equals protection in numbers, so a lack of the need of protection equals a lack in the need to school. For another, caves have scarcer food. Groups eat more and eat together. When there is less food and it is more spread out it is advantageous to find and eat it alone. Put together, this relaxed the selective pressure on schooling behavior causing multiple genetic changes, only some of which are vision-dependent.


Johanna E. Kowalko, Nicolas Rohner, Santiago B. Rompani, Brant K. Peterson, Tess A. Linden, Masato Yoshizawa, Emily H. Kay, Jesse Weber, Hopi E. Hoekstra, William R. Jeffery, Richard Borowsky, & Clifford J. Tabin (2013). Loss of Schooling Behavior in Cavefish through Sight-Dependent and Sight-Independent Mechanisms Current Biology, 23, 1874-1883 DOI: 10.1016/j.cub.2013.07.056

See also:

Alison M. Bell (2013). Evolution: Skipping School Current Biology, 23 (19) DOI: 10.1016/j.cub.2013.08.022

Anna K. Greenwood, Abigail R. Wark, Kohta Yoshida, & Catherine L. Peichel (2013). Genetic and Neural Modularity Underlie the Evolution of Schooling Behavior in Threespine Sticklebacks Current Biology, 23 (19), 1884-1888 DOI: 10.1016/j.cub.2013.07.058


(images via Seriously Fish)